Patterns of range use, range defense, and intergroup ... - Springer Link

PRIMATES,34(1): 11-25, January 1993

11

Patterns of Range Use, Range Defense, and Intergroup Spacing in Moustached Tamarin Monkeys

(Saguinus mystax) E A. GARBER, J. D. PRUETZ, a n d J. ISAACSON

University of Illinois

ABSTRACT. In this paper we examine patterns of group spacing and habitat utilization in neighboring groups of marked free-ranging moustached tamarin monkeys (Saguinus mystax) inhabiting Padre Isla, a small island in the Amazon Basin of northeastern Peru, and describe the set of behavioral mechanisms used by tarnarins to maintain the spatial isolation and social integrity of individual groups. Specifically, we address a series of questions regarding the importance of resource defense, mate defense, and territorial defense in intergroup interactions. From June through November 1990, we recorded 67 intergroup interactions involving members of our two main study groups. These interactions occurred at a rate of .14/observation hour and were of two general types. Vocal battles averaged 18 min in duration and were characterized by a series of high frequency, short syllable, long calls that were exchanged between groups separated by distances of greater than 25 m. Aggressive encounters averaged 26 min in duration and involved visual contact, alarm calls, scent marking, and sequences of chases and retreats. Intergroup confrontations did not cluster around the perimeter of a group's home range, and there was no evidence that moustached tamarins patrolled range borders. Our data indicate that 35~ of aggressive encounters occurred in the vicinity of major feeding trees. Priority access to these sites is likely to have an important influence on tamarin foraging success. Mate defense and the exploration of new breeding opportunities also appear to be important functions of intergroup conflicts. Not only did the frequency of aggressive encounters increase during breeding periods, but three-fourths of all observed copulations occurred during or within 30 min of an encounter. Given the high degree of reproductive competition reported among tamarin females and the time and energy group members devote to intergroup aggression, maintaining access to a stable home range and the resources contained within that range appear to be critical functions of moustached tamarin social interactions. Key Words: Saguinus mystax; Tamarin monkey; Territorial behavior; Resource defense; Group spacing.

INTRODUCTION F i e l d d a t a o n p a t t e r n s o f g r o u p spacing in New W o r l d p r i m a t e s indicate t h a t m a n y species actively d e f e n d p a r t or all o f their h o m e range a g a i n s t incursions by n e i g h b o r i n g conspecific groups. S e p a r a t i o n is enforced t h r o u g h a variety o f spacing m e c h a n i s m s including a v o i d a n c e a i d e d by l o u d calls (e.g. Alouatta seniculus; CROCKETT & EISENBERG, 1987), aggressive defense o f i m p o r t a n t feeding sites (e.g. Cebus olivaceus; ROBINSON & JANSON, 1987), defense o f fixed core areas within the range (e.g. s o m e g r o u p s o f Cebus capucinus; OPVENHEIMER, 1982), a n d active p a t r o l o f range b o r d e r s (e.g. m a l e Ateles paniscus; VAN ROOSMALEN & KLEIN, 1988, a n d m a l e a n d female Leontopithecus rosalia; PERES, 1986). I n m o n o g a m o u s t a x a such as Callicebus moloch, Callicebus torquatus, a n d Aotus sp., h o m e ranges represent areas o f exclusive use (ROBINSON, 1981; EASLEY, 1982; WRIGHT, 1985). A l t h o u g h p a t t e r n s o f range use a n d range defense v a r y between callicebine species, vocal

12

P.A. GARBERet al.

exchanges typically occur at territorial boundaries and involve coordinated duetting and/or aggression by the resident male-female pairs. It is suggested that duetting and behaviors associated with duetting serve an important function in maintaining pair proximity, reinforcing sociosexual bonds, and insuring the integrity of a monogamous mating system (ROBINSON et al., 1987). Tamarins of the genus Saguinus also have been described as territorial (DAWSON, 1979; TERBORGH, 1983; NORCONK, 1986; GOLDIZEN, 1987; SOINI, 1987; SNOWDON& SOINI, 1988). In contrast to Aotus and Callicebus, however, home range overlap in Saguinus is more extensive (usually from 20% to over 40%0), vocal duetting is absent, and calls given by a resident group often act to increase rather than decrease the likelihood of an encounter. Although the response given to a neighboring group can be highly variable, in species such as Saguinus geoffroyi (DAWSON, 1979), S. oedipus (NEYMAN, 1977), S. fuscicollis (TERBORGH, 1983; CRANDLEMIRE-SAcco, 1986; GOLDIZEN, 1987), S. imperator (TERBORGH, 1983), S. labiatus (BuCHANAN-SMITH, 1991; BUCHANAN-SMITH & JORDAN, 1992), and S. mystax (NoRCONK, 1986; RAMIREZ, 1989; CASTRO, 1991) intergroup conflicts may occur every few days and last for more than one hr. The frequency of encounters, and the time and energy spent in intergroup aggression suggest that maintaining access to a stable home range and resources contained within that range is a critical part of tamarin social interactions. In this paper we examine social interactions between neighboring groups of free-ranging moustached tamarin monkeys (Saguinus mystax) in an attempt to identify (1) the set of factors that serve to attract groups into the same area and (2) the set of behavioral mechanisms used to maintain and reinforce the spatial isolation and social integrity of these groups. Specifically, we explore a series of questions regarding the possible functions of intergroup confrontations. These questions address: (1) the spatial association between the location of intergroup conflicts and the location of major feeding trees (resource defense); (2) the temporal relationship between the frequency of intergroup encounters and periods of female receptivity (mate defense); and (3) the degree to which groups maintain spatial exclusivity by defending the boundaries of their range (territorial defense). Evidence of temporal and spatial differences in intergroup encounters provides a meaningful framework for examining factors that influence patterns of range use, social cohesion, and group spacing in primates.

METHODS

STUDY SITE From June through November 1990, 476 hr of quantitative data were collected on the social behavior and feeding ecology of two marked groups (Copper group and Green group) of moustached tamarin monkeys inhabiting Padre Isla, a small island (5.2 km 2) in the Amazon basin of northeastern Peru ($3~ W73~ Moustached tamarins are not native to the island. Between 1977 and 1980 researchers from the Proyecto Peruano de Primatologia and the Ministerio de Agricultura y Alimentaci6n wild-trapped and released 20 S. mystax groups (87 animals) on Padre Isla for study. The island is composed of a series o f narrow and somewhat isolated forested areas (restingas) separated by a complex system o f lagoons (cochas) (MoYA et al., 1980). Although water barriers serve as natural boundaries between group ranges, both individual migrants and entire groups occasionally cross

Intergroup Encounters in Tamarin Monkeys

13

from one restinga to another. None of the groups on the island were provisioned during our study, nor have they been provisioned in the past. In 1990 the tamarin population of Padre Isla was retrapped and recensused. The present population totals 123 animals residing in 17 social groups (GARBER et al., in press). Mean group size was 7.0, including 2.2 adult males and 2.0 adult females per group. In terms of demographic structure, population density, and the size and composition of individual social groups, the moustached tamarin population on Padre Isla is indistinguishable from that reported for moustached tamarin groups in other areas of Peru (SOINI& SOINI, 1982; SUSSMAN& GARBER, 1987; SNOWDON & SOINI, 1988; GARBER et al., in press).

DATA COLLECTION Information on moustached tamarin diet, habitat utilization, and social interactions was collected on marked individuals in each study group using a 2-min instantaneous focal animal time sampling technique (point sample). Prior to focal animal sampling, group members were trapped, examined, aged, and fitted with stainless steel ball-chain collars. Each collar contained a unique sequence of three colored beads to facilitate the recognition o f individual animals in the field (see GARBER et al., in press for a more detailed account of trapping and data collection methods). In order to address questions regarding intergroup spacing, patterns of habitat utilization, resource distribution, and ranging, a trail system was constructed throughout the home range of each study group. The locations of trail markers, feeding trees, and sleeping sites were mapped using a Brunton transit mounted on a tripod. The coordinates of these 480 points were digitized into the Geographical Information System (CERYL) at the University of Illinois. A 25m grid (.0625 ha quadrats) was superimposed on the field map, and a series of plots showing tamarin ranging patterns and the distribution o f feeding sites were generated. H o m e range size for each group was determined by constructing a polygon connecting the outermost distribution of feeding trees, resting sites, and the locations of intergroup encounters. This measure tends to underestimate total range size since it does not include areas exploited during a small number of brief excursions in which members of the study groups used seasonally available travel routes to cross between adjacent restingas. The area of home range overlap between the two study groups (Green and Copper) was calculated as the smallest polygon that encompassed feeding and resting sites used in common by both groups. During intergroup conflicts we recorded the location of group members, the identity of the participants, and patterns o f social interactions. The length o f each conflict (aggressive encounter or vocal battle) was scored as the total number of minutes during which group activity was directed toward members of another social group. These activities included chasing, vocalizing, scent marking, fighting, displaying, vigilance, and fleeing. The proportion of the home range associated with intergroup encounters was determined by calculating the total area contained in a circle radiating 25m from the center of each conflict. Twenty-five meters represents an estimate of the maximum canopy sighting distance from which groups exchanged visual threats. The area contained within this circle is referred to as the " z o n e of active conflict." To determine whether the location o f intergroup encounters was influenced by the location of important feeding sites, two sets of feeding trees were identified. Major feeding sites were defined as the set of individual trees that accounted for the top 50% of plant feeding

14

R A. GARBERet al.

time during each m o n t h of the study. These trees generally fruited over a period of several weeks and were a m a j o r focus of group activity. Trees visited infrequently or exploited during extremely brief feeding bouts ( < 2 min) were classified as minor feeding sites. For each intergroup encounter, we identified the number of major feeding trees that were visited the previous week and located in the " z o n e of active conflict." A chi-square test was used to evaluate the hypothesis that the frequency of intergroup conflicts was significantly greater in quadrats containing major feeding trees than in quadrats in which major feeding trees were absent.

RESULTS GROUP SIZE, COMPOSITION, AND MATING PATTERNS

The two groups selected for study (the Copper group and the Green group) inhabited overlapping ranges on the Central Restinga of the island (Fig. 1). This area is characterized by undisturbed lowland forest as well as chacras or cultivated fields. When first encountered (June), the Copper group was a unisexual group containing two adult females (green female and red female) and one subadult female (yellow female). The green female was released onto the island as an adult in 1980, and thus was at least 12 years of age in 1990. The three females of the Copper group traveled, fed, rested, and interacted as a single cohesive social unit. On September 24, one adult male (yellow male) and one subadult male (green male) joined the group. These males had been trapped and marked earlier in the study (August), when they were members of an established group of six animals (Blue group) located on an adjoining restinga. Their inclusion into the group was rapid and without any indication of aggression or conflict. This newly formed bisexual group remained together for the duration of the study (Table la). The second study group, Green, contained one adult female, three adult males, and two infant males. Copulations in the Copper group between each immigrant male and the oldest female

Home Range Area of Moustached Tamarin Study Groups, Padre Isla, Peru

N

I ....... 50meters

* Copper/Green common feeding trees 9 Copper group sleeping trees [] Green group sleeping trees [] Copper/Green common sleeping tree Fig. 1. Home range of the Copper and the Green groups. Area of home range overlap includes feeding and sleeping sites used in common by both groups.

15

Intergroup Encounters in Tamarin Monkeys Table la. Group size and composition. Group

Adult male

Adult female

Subadult male

Subadult female

Infant

Total

Copper Green

1 3

2 1

1 0

1 0

0 2

5 6

Table lb. Mating activities in the two groups. Group Copulations observed Copper Yellow male with green female Green male with green female Yellow male with unidentified female Yellow male with red female Green Silver male with purple female White male with purple female White male with purple female Red male with purple female

(green female) were observed during the first week of group formation (Table lb). Two additional Copper group matings were recorded four weeks later. One of these involved the adult male (yellow male) and a second adult female (red female). Given that more than one female and more than one male were sexually active, the mating pattern of this group is provisionally described as polygynous. Four copulations were observed in the Green group. The lone female (purple female) of the group copulated with the white male on two occasions, with the red male on one occasion, and with the silver male on one occasion (Table lb). Copulations by different males with the purple female were observed to occur within as brief a span as 42 min. The mating pattern of the Green group is considered polyandrous. There was no evidence of mate guarding or aggressive competition for access to reproductive partners among members of the same social group. PATTERNS OF R A N G I N G AND HABITAT UTILIZATION

During the five months of this study the Copper group occupied an area o f 6.8 ha and was observed to feed in 107 individual trees. Sixteen of these (15%) were classified as major feeding trees (i.e. trees that accounted for the top 50% of the tamarin diet in any 1 month period) and 91 (85%) were classified as minor feeding trees. O f the major feeding trees, 12 were legumes of the genus Inga and 2 were figs. Thirteen percent of the trees visited by the Copper group were also fed in by the Green group (six major trees and eight minor trees). Trees visited in c o m m o n were located in an area of forest and chacra totaling 2.6 ha (this included 19 overlap quadrats located in the boundary zone). Thus, 38% of the home range occupied by the Copper group contained feeding sites and sleeping sites that were also utilized by the Green group. Given the limited amount of time the Green group was followed (95 hr o f observation over 25 days), it is not possible to provide an accurate assessment of total range size and the number of feeding trees exploited. Based on our observations of ranging, feeding, and foraging activities, we estimate that this group utilized an area of approximately 15 ha. In this area we identified 42 feeding trees and 5 sleeping sites. Figure 1 illustrates the size of each group's home range, the area of range overlap, and feeding trees and sleeping sites used in common. The Copper group was observed to enter a total of 109 different 25 x 25m quadrats

16

P.A. GARBERet al.

Table 2. Patterns of home range exploitation and intergroup encounters in Saguinus mystax. No. Area Home range Activity No. major No. intergroup Zone quadrats (ha) (%) budget (%) feedingtrees conflicts~ Central 21 1.3 19.3 39.8 6 11 Overlap 22 1.4 20.2 43.4 4 27 Boundary2~ 66 4.1 60.5 16.8 6 22 Total 109 6.8 100 100 16 60 1) The numbers represent only intergroup interactions that occurred within the home range of the COPPER group; 2) the boundary includes 19 quadrats that were areas of overlap and used by more than one group.

(Table 2). Range use was not uniform, however, with 38.8% o f the activity budget restricted to only 5 quadrats (0.3 ha), and 88% of the activity budget restricted to a total of 29 quadrats (1.8 ha). Forty-five percent of the most heavily utilized quadrats (in which the group spent at least 1% of activity time) were located in the central part of the range, 34.5% in the overlap zone, and 20.7% in the boundary zone (Fig. 2). The five most frequently used quadrats ( > 5 % of activity time) were located in the central and overlap zones. Major feeding trees exploited by the Copper group were scattered throughout the group's h o m e range (Fig. 3). This is evidenced by the fact that the number of these trees in the central, overlap, and boundary zones did not differ significantly from that expected based on the size of each area (X2=4.5, d.f. =2, p > . 0 5 ; Table 2). Members of the Copper group exhibited the general moustached tamarin dietary pattern of concentrating their feeding efforts on a large number of individual trees from a small number of plant species each day. Despite small group size, the number of feeding trees visited per day ranged from 5 to 23 ( ~ = 1 2 . 2 _ 3 . 9 ) . Mean feeding bout length was 5.2 min__+2.08 (N=495 feeding bouts). INTERGROUP INTERACTIONS During the study we recorded 67 intergroup interactions. Forty-four of these conflicts were between the Copper and the Green groups. The remaining conflicts involved members of either the Copper group or the Green group with one of five neighboring groups. These interactions occurred at a rate of .14/observation hr, included active participation by adults of both sexes, and were of two general types (Table 3). Vocal battles were characterized by a series of high frequency, short syllable, long calls that were exchanged between groups separated by physical barriers (cochas) or distances of greater than 25 m. Bouts of long calling averaged 18.0 min in duration (Table 3) and occurred principally during the first 2 hr o f exiting the sleeping tree. Only two vocal battles (5.5%) were recorded after 12:00 noon. The second type of intergroup interactions were termed aggressive encounters. These were agonistic in nature and characterized by visual contact, alarm calls, scent marking, threatening postures, and sequences of aggressive chases and rapid retreats. Chases and retreats took place both on the ground and in the canopy. After such an encounter, the competing groups occasionally remained in the immediate area and rested in trees located 5 0 - 1 0 0 m apart. Fifty-two percent of aggressive encounters (N=16) began as a vocal battle, with the exchange of long calls between distant groups. These long calls, however, failed to maintain or increase the distance between the groups and were a prelude to agonistic confrontation. In the remaining 15 cases the sequence differed only in that visual contact and alarm calls


17

HOME RANGEOF COPPER GROUP - PADRE ISLA B B B B B B B B B B B B B B 0,8 o,. o,B o,B B B B B B [] [] , ~ , ~ l ~ : ~ l ~ o , B o,B o,B B B ~D~,~'~" o;;~ o 5 -< 11 percent of activity budget

[]

>_ 1 < 5 percent of activity budget

[]

< t percent of activity budget

= QUADRATSOFNOMERANGEOVERLAP

Fig. 2. Home range of the Copper group indicating areas designed as boundary, overlap, and central quadrats. Shading indicates the percent time active in each quadrat (night time resting is excluded from the calculations).

DISTRIBUTION OF MAJOR FEEDING TREES AND LOCATIONS OF INTERGROUP CONFLICTS IN THE HOME RANGE OF THE COPPER GROUP- PADRE ISLA

_

H

~

X

X H

~

H

X

I

.

H x

X

H

X

X

H H

e

X x

X

X

:X X

x x

I.I Fig. 3. A comparison of the location of intergroup conflicts, the location of the central area, and the location of quadrats containing at least one major feeding tree in the home range of the Copper group. Darkened or bordered area within the home range represents the "central area," which is an area of relatively exclusive use. ~ : Quadrats containing major feeding trees; , : locations of intergroup conflicts.

were initiated without prior long calls. Aggressive encounters lasted an average o f 25.2 min (Table 3), and as in the case o f vocal battles occurred principally in the early morning. O n only one occasion did an intergroup c o n f r o n t a t i o n result in aggressive physical contact between participants. In two other instances, groups were in visual contact but exhibited no overt indication o f aggression or hostility. Intergroup interactions accounted for 5~ o f activity time. WASER (1987) has proposed a model to predict the frequency with which neighboring

18

P. A. GARBERet al.

Table 3. Agonistic intergroup interactions in moustached tamarins. Period (week) 1 ( 1 - 11) 2(12-19) 1+ 2

Rate of vocal Mean length of Rate of Mean length Rate of all No. vocal battles vocal battles No. of encounters of encounters interactions battles (per hr) (rain) encounters (per hr) (rain) (per hr) 22 14 36*

.06 .11 .08

22.7 10.7

16 15

18.0

31 *

.05 .12 .07

16.4 38.0 25.2

.11 .23 .14

9 Total number of Period 1 through 2.

groups are expected to encounter one another by random movements and chance associations between groups exploiting areas of common use. The expected frequency of encounters (Z) is equal to:

N ~/(Vi 2 + Vj2)pj r, where N represents the number of overlapping groups, pj is the density of tamarin groups on the island (groups per m2), r is the mean radius of the spread of each group plus the distance between groups beyond which they are assumed not to be in association, and vi and vj equal the average rate o f travel (m/hr) for each group. Given the density of moustached tamarin groups on Padre Isla (17 groups/5.2 km2), the average rate of hourly travel (33 m / h r based on data collected by NORCONK, 1986, on 2 groups of moustached tamarins on Padre Isla), the number of groups that overlap with the Copper group (N= 5), average group spread (10m), and the distance beyond which 2 groups were considered not to be in association (25m); the encounter rate expected by chance associations is .034/hr. The rate of aggressive encounters observed in our study groups (.065/observation hr) was two times greater than that expected by chance alone. In order to identify factors that contributed to this high rate of encounter, we examined the function of resource defense, mate defense, and territorial defense in intergroup spacing. Resource Defense If intergroup conflicts are resource related, then a greater than expected number of confrontations should occur in quadrats containing major feeding sites. An examination of the location of intergroup conflicts indicates that 35% (11/31) of aggressive encounters and 25% (9/36) of vocal battles occurred within 25 m of a major feeding tree. Given that only 12% of the quadrats in the Copper group's home range contained major feeding sites and 30o/o of all intergroup conflicts occurred in these areas (X2= 18.0, d.f. = 1, p < .001), defending or maintaining access to productive feeding trees is likely to be an important function of intergroup interactions. Rather than guarding or monitoring these feeding sites, however, moustached tamarin groups appear to be independently attracted to productive feeding sites located in boundary zones and areas of range overlap (Fig. 3). This is supported by our observations that moustached tamarins rarely remain in the vicinity of a major feeding tree after eating, and that over 56% of all major feeding trees were located in quadrats in which aggressive encounters were not preceded by vocal advertisement or long calls. Mate Defense If intergroup encounters are associated with aspects of reproductive competition, mate


19

guarding, and/or opportunities for extragroup copulations, then the frequency of such encounters is likely to be greater during periods of female receptivity than during periods when females are not sexually active. In order to test this possibility, we divided our data set into two relevant periods of observation. Period 1 represents an ll-week period (July 1 through September 23) in which no member of either study group was observed to copulate. Period 2 represents an 8-week period (September 24 through November 20) in which copulations were observed in both study groups. As illustrated in Table 3, the rate of intergroup confrontations during Period 1 was .ll/hr. During period 2 the confrontation rate doubled to .23/hr, with both the number of vocal battles and aggressive encounters increasing. Differences in the rate of confrontation between these two periods were significant (Mann-Whitney U-test: Z = 2.27, N = 19, p < .02). In addition, the mean duration of aggressive encounters during Period 2 (38.0 min) was more than double that recorded for Period 1 (16.4 min; Mann-Whitney U-test: Z=2.08, N = 3 0 , p.05). There is evidence to suggest that intrasexual competition was an important factor motivating intergroup aggression. Of the eight copulations we observed in Period 2, two occurred during an intergroup encounter, three occurred within 30 rain of an intergroup encounter, and one occurred during a vocal battle that led to an intergroup encounter. Moreover, on the same day that the white male was observed to copulate in the Green group, he was also seen in close, nonaggressive physical contact with two females (green female and yellow female) of the Copper group. These females inspected the male before he was threatened and driven off by the resident male (yellow male) of the Copper group. On three other occasions the oldest female (green female) in the Copper group was attacked repeatedly by the oldest male (yellow male) of her group as she nonaggressively approached a male of the Green group. These attacks may have served to keep this female in her present group and prevent her from transferring into the neighboring group.

Territorial Defense In order to maintain exclusive access to space, resting sites, and food resources, intergroup conflicts are expected to occur principally along boundary zones rather than in more central areas of the range. Monitoring of boundary zones requires a ranging pattern in which vigilance or patrolling behavior is directed towards the perimeter. Is there evidence that moustached tamarins monitor and defend territorial boundaries? This question was examined by comparing the spatial proximity of aggressive encounters and vocal battles to the perimeter of the Copper and the Green groups' home ranges. The perimeter was defined as the total area contained within 25 m o f the border o f a group's range. Agonistic interactions that occurred within the perimeter area were considered to serve a territorial function; that is to prevent other groups from entering into the range. To determine the degree to which "zones of active conflict" were concentrated in border quadrats, we divided the home range of the C O P P E R group into three areas of utilization: (1) A zone in the interior of the range that represented an area of relatively exclusive use. It is analogous to the concept of "isolation field" defined by WASER and WILEY (1979), and we refer to this as the central area; (2) a shared area of overlap within the ranges of the Copper and the Green groups; and (3) an area around the perimeter of the home range that was designated the boundary zone.

20

P.A. GARBERet al.

Our data indicate that although 36% of vocal battles and aggressive encounters were located in boundary quadrats, this is significantly less than expected based on the number of boundary quadrats in the Copper group's home range (Table 2: X2= 5.6, d.f. = 1, p > .02). The Green and the Copper intergroup agonistic interactions did not cluster along range borders, and there was no evidence that group members actively patrolled perimeter zones. In fact, the Copper group spent a smaller proportion of its activity time in boundary quadrats than expected based on the size o f this area relative to both central and overlap zones (Table 2: X2= 79.8, d.f. = 2, p < .001). Patterns of home range use in these moustached tamarins do not support the contention that intergroup conflicts are principally territorial in nature.

DISCUSSION Established groups of many, if not all, species of tamarins are reported to occupy stable ranges that are defended against neighboring conspecific groups (DAwsoN, 1977, 1979; NEYMAN, 1977; SOINI & SOINI, 1982; TERBORGH, 1983; CRANDLEMIRE-SAcco, 1986; NORCONK, 1986; GARBER, 1988; RAMIREZ, 1989; BUCHANAN-SMITH & JORDAN, 1992). Despite frequent vocal battles and aggressive encounters, group ranges overlap considerably and feeding sites located in areas of overlap are often exploited by more than one of the resident groups (CRANDLEMIRE-SAcco,1986; NORCONK, 1986; GARBER, 1988; RAMIREZ, 1989). In this regard, NORCONK (1986) has suggested that tamarin home ranges are best described as a combination of shared overlap zones and exclusive territories. Both of these areas, however, are defended in the presence of a conspecific group. Given evidence that the location and the frequency of intergroup interactions may vary throughout the year (DAWSON,1977, 1979; NORCONK, 1986; GARBER, 1988; RAMIREZ, 1989), or differ in intensity depending on the neighboring groups involved (DAWSON,1979; SAVAGE,1990; CASTRO, 199i), simple distinctions between territorial and nonterritorial species provide little insight into the specific behavioral and ecological factors that influence intergroup spacing and social cohesion. Data presented in this study of neighboring groups of moustached tamarins indicate that intergroup conflicts are likely to serve a variety of functions including the defense of feeding sites, defense of an area in the group's immediate vicinity, and defense of mates. Evidence in support o f these conclusions is as follows: 1) Approximately 30% of all conflicts between the Copper and the Green groups occurred within 25 m of a major feeding tree. In many instances it was not possible to determine whether groups were mutually attracted to the same food resource or simply attracted to the presence of the other group. The results of these battles, however, were to enable one of the competing groups to achieve first or priority access to important feeding sites. Data collected on resource defense in other tamarin populations support this contention (GARBER, 1988). In a study of a mixed species association of S. mystax and S. fuscicollis, GARBER (1988) found that changes in the location of intertroop encounters were closely associated with changes in the locations of major feeding trees. Given the widespread distribution of major feeding trees throughout the troop's 40 ha home range, benefits associated with resource defense were substantial. When successful in defending a major feeding tree, members of a mixed species troop traveled significantly shorter distances to encounter the next major


21

feeding site (59 m vs. 331 m; GARBER, 1988). GARBER (1988) argues that advantages associated with cooperative resource defense may be one of the most important factors maintaining the stability of tamarin mixed species troops. In contrast, NORCONK (1986) found a negative correlation between the number of feeding trees'per quadrat and the location of intertroop encounters in her study of a mixed species troop of moustached and saddle-back tamarins. Although 4307o of intertroop interactions occurred while her main study troop was feeding, the negative correlation led her to conclude that resource defense was not a primary function o f these encounters. In our study on Padre Isla, the relationship between the number of feeding trees per quadrat and the location of intergroup interactions also was not significant (Rs=13, p > . 1 9 , N=109). When the data for major and minor feeding trees were analyzed separately, however, the results were significant, indicating a strong positive correlation between quadrats containing major feeding trees and quadrats in which intergroup interactions were frequent (Rs=.20, p < . 0 4 , N = 109). In several callitrichine species, there is evidence that neighboring groups compete for access to productive feeding trees located in shared areas of their range (DAWSON, 1979; CRANDLEMIRE-SAcco, 1986; RYLANDS, 1986; PERES, 1986; GARBER, 1988; STEVENSON& RYLANDS,1988; RAMIREZ,1989). The ability of one group to dominate its neighbor at these feeding sites is likely to be a critical factor in foraging success. 2) Several authors have suggested that tamarin long calls serve to advertise and defend the integrity of the home range (TERBORGH, 1983; NORCONK, 1986; SNOWDON & SOINI, 1988). These calls are given principally in the early morning and are generally assumed to increase or maintain the distance between groups. In 3107o of the vocal battles between our study groups, however, long calls served to provoke an aggressive face-to-face encounter, l_~ng distance vocalizations by either tamarin group were only partially effective in maintaining exclusive access to space or resources. Why these vocalizations act to avoid conflict on certain occasions and promote conflict on other occasions remains unknown. In 65~ of the vocal battles (15/23) that did not lead to an encounter, the interacting groups were separated by a physical barrier such as a lagoon or zone of discontinuous forest. These areas served as natural boundaries and were difficult for the tamarins to cross. In the remaining eight cases (five from Period 1 and three from Period 2; three located in central quadrats, three located in overlap quadrats, and two located in border quadrats), we were unable to identify any factor or set of factors that kept either group from approaching the other. Although it can be argued that the small size and narrow configuration of the Copper group's home range may have influenced the frequency and intensity of intergroup interactions, the rate of moustached tamarin long calls on Padre Isla was comparable to the rate of long calls reported for a natural population of moustached tamarins at the Rio Blanco Field Site (NORCONK, 1986). In general, rather than patrolling or defending fixed territorial borders, intergroup conflicts in moustached tamarins functioned to maintain the space around, and the integrity of the social group. 3) Mate defense and the exploration of new breeding opportunities also appear to be important functions of tamarin intergroup encounters (GOLDIZEN, 1987; BUCHANAN-SMITH & JORDAN,1992). Three-fourths of the copulations we observed occurred during or within 30 min of an intergroup encounter. Moreover, the increased rate of intergroup contacts recorded for Period 2 coincided with a breeding period. Moustached tamarins are reported to be seasonal breeders with the primary copulatory period from July through October (SNoWDON & SOINI, 1988). If the Green or the Copper group female(s) were ovulating,

22

P.A. GARBERet al.

then competition for access to extragroup sexual partners may have influenced the high rate of intergroup conflicts that occurred during Period 2. It is also possible that sexual arousal is heightened during intergroup encounters. The copulations we observed may have represented a form of mate guarding as well as the reinforcement of sociosexual bonds between group members. HUBRECHT(1985) reports a case of extragroup copulations in the common marmoset (Callithrix jacchus). These copulations occurred during an encounter between neighboring groups and involved a young female and one or more males. Given the amount of time and energy resident male callitrichines devote to communal care of the group's young, behaviors designed to guard against the possibility of cuckoldry are likely to be well developed. Demographic data collected on Saguinus fuscicollis (GOLDIZEN t~ TERBORGH, 1989; GOLDXZEN, 1990), S. geoffroyi (DAWSON, 1977), and S. oedipus (SAVACE, 1990) indicate the possibility that intergroup encounters may facilitate the transfer of migrants into nearby groups. In these species there is evidence that several immigrants into the main study groups had previously resided in neighboring groups. Although the processes associated with intergroup transfer are not well documented, our observation of what may have been an attempt by the green female of the Copper group to transfer into the Green group is similar to RYLANDS' (1982) description of an intergroup encounter in which an adult female tasselear marmoset (Callithrix humeralifer) attempted to enter a neighboring group. Female transfer during intergroup interactions has been reported in other primate species such as the mountain gorilla (Gorilla gorilla: HARCOURT, 1978; WATTS, 1990), the capped langur (Presbytis pileata: STANFORD, 1991), and the mantled howler monkey (Alouatta palliata." MILTON, 1982). Moreover, as reviewed by PUSEY and PACKER (1987), in primate species exhibiting direct transfer, individuals generally migrate into neighboring groups. In callitrichine primates (excluding perhaps Goeldi's monkey, Callimico goeldii: MASATAKA, 1981), female reproductive competition is extremely high, and only the dominant female in each group produces offspring (ABBOTT, 1984; KNOX & SADE, 1991; GARBER et al., in press). A female also requires the presence of adult helpers to assist in the care and transport of her young. The specialized nature of tamarin and marmoset social and breeding systems has resulted in a demographic situation in which the number of breeding females in the population rarely exceeds the number of social groups that can establish and maintain access to a stable range. In theses species, range acquisition and the maintenance of spatial and social isolation between neighboring groups appear to be prerequisites for successful reproduction (NoRCONK, 1986). In conclusion, interactions between neighboring groups of tamarins are complex and include indifference, avoidance, vocal exchanges, and aggressive confrontations. Although conspecific groups have been observed to merge temporarily or feed jointly at the same feeding site, in only one species, S. nigricollis, is this reported to occur frequently (IZAWA, 1978). The particular response given to conspecific groups may vary depending on the size and composition of each group, previous opportunities to form an alliance with members of neighboring social group, kinship, proximity to important resources, overall resource availability, and reproductive opportunities. Despite difficulties in distinguishing which of these factors is the primary determinant of any single intergroup interaction, evidence of temporal and spatial differences in the frequency and intensity of encounters has provided a meaningful framework for examining the functions of intergroup encounters in moustached tamarin monkeys.


23

Acknowledgments. Permission and logistical support required to conduct this research were provided by Dr. JA1MEMORO (Director of the Instituto Veterinario Investigaciones Tropical y Agronomia, Dr. FILOMENO ENCARNACION(Director of the Proyecto Peruano de Primatologia), and Dr. Luls MOYA (Ministerio de Agricultura y Alimentaci6n). We gratefully acknowledge their contribution to this project. We also wish to thank Josl~ OSCANOALAGUNAS,DIDIER LAMY, WALTER MERMAO, ERIBERTO MERMAO, CARLOSIQUE, and WALTER VASQUEZfor their assistance in collecting data in the field. Plant species were identified in the field by Dr. FRANKLYNAYALAand JUAN RUIZ of the Departamento de Ecologia Vegetal, Universidad Nacional de la Amazonia Peruana. Critical comments on earlier drafts of the manuscripts were provided by LYNETTE NORR. This research was supported by grants from the National Geographic Society and the Research Board of the University of Illinois.

REFERENCES ABBOTT, D. H., 1984. Behavioral and physiological suppression of fertility in subordinate marmoset monkeys. Amer. J. PrimatoL, 6: 169-186. BUCHANAN-SMITH, H. M., 1991. Encounters between neighbouring mixed species groups of tamarins in northern Bolivia. Primate Report, 31: 9 5 - 9 9 . & T. R. JORDAN, 1992. An experimental investigation of the pair bond in the callitrichid monkey, Saguinus labiatus. Int. J. Primatol., 1 3 : 5 1 - 7 2 . CASTRO, N. R., 1991. Behavioral ecology of two coexisting tamarin species (Saguinus fuscicollis nigrifrons and Saguinus mystax mystax, Callitrichidae, Primates) in Amazonian Peru. Ph.D. thesis, Washington Univ., St. Louis, Missouri. CRANDLEMIRE-SAcco, J. L., 1986. The ecology of the saddle-back tamarin, Saguinusfuscicollis, of southeastern Peru. Ph.D. thesis, Univ. of Pittsburgh, Pittsburgh, Pennsylvania. CROCKETT, C. M. & J. E EISENBERG, 1987. Howlers: variations in group size and demography. In: Primate Societies, B. B. SMUTS, D. L. CHENEY, R. M. SEYFARTH, R. W. WRANGHAM, & T. T. STRUHSAKER (eds.), The Univ. of Chicago, Chicago, pp. 5 4 - 6 8 . DAWSON, G. A., 1977. Composition and stability of social groups of the tamarin, Saguinus oedipus geoffroyi, in Panama. In: The Biology and Conservation of the Callitrichidae, D. G. KLmMAN (ed.), Smithsonian Univ. Press, Washington, D.C., pp. 2 3 - 38. - - , 1979. The use of time and space by the Panamanian tamarin, Saguinus oedipus. Folia Primatol., 31: 253-284. EASLEY, S. P., 1982. Ecology and behavior of Callicebus torquatus, Cebidae, Primates. Ph.D. thesis, Washington Univ., St. Louis, Missouri. GARBER, P. A., 1988. Diet, foraging patterns, and resource defense in a mixed species troop of Saguinus mystax and Saguinus fuscicollis in Amazonian Peru. Behaviour, 105: 18-34. - - , E ENCARNACION, L. MOYA, & J. D. PRUETZ, in press. Demographic and reproductive patterns in moustached tamarin monkeys (Saguinus mystax): implications for reconstructing platyrrhine mating systems. Amer. J. Primatol. GOLmZEN, A. W., 1987. Tamarins and marmosets: communal care of offspring. In: Primate Societies, B. B. SMUTS,D. L. CHENEY, R. M. SEYFARTH,R. W. WRANGHAM,& T. T. STRUHSAKER (eds.), The Univ. of Chicago, Chicago, pp. 3 4 - 4 3 . - - , 1990. A comparative perspective on the evolution of tamarin and marmoset social systems. Int. J. Primatol., 11: 6 3 - 83. & J. TERBORGH, 1989. Demography and dispersal patterns of a tamarin population: possible causes of delayed breeding. Amen Naturalist, 134: 2 0 8 - 224. HARCOURT, A. H., 1978. Strategies of emigration and transfer by primates, with particular reference to gorillas. Z. Tierpsychol., 4 8 : 4 0 1 - 4 2 0 . HUSRECHT, R. H., 1985. Home-range size and use and territorial behavior in the common marmoset, Callithrixjacchus jacchus, at the Tapacura field station, Recife, Brazil. Int. J. Primatol., 6:533 - 550. IZAWA, K., 1978. A field study of the ecology and behavior of the black-mantle tamarin (Saguinus nigricollis). Primates, 19:241-274. KNox, K. L. & D. S. SADE, 1991. Social behavior of the Emperor Tamarin in captivity: components of agonistic display and agonistic network. Int. J. Primatol., 12: 439-480. -

-

-

-

24

P . A . GARBER et al.

MASATAKA,N., 1981. A field study of the social behavior of Goeldi's monkeys (Callimico goeldil) in North Bolivia. I. Group composition, breeding cycle, and infant development. Kyoto Univ. Overseas Res. Rep. of New World Monkeys, 2: 2 3 - 41. MILTON, K., 1982. Dietary quality and demographic regulation in a howler monkey population. In: The Ecology of a Tropical Forest." Seasonal Rhythms and Long-term Changes, E. G. LEIGH, JR., A. S. RAND, • D. M. WINDSOR (eds.), Smithsonian Institution Press, Washington, D.C., pp. 273 - 289. MOYA, L., M. TRIGOSO, & P. G. HELTNE, 1980. Manejo de fauna silvestre en semicautiverio en la Isla de Iquitos y Padre Isla. - Afio 1980. Informe Ordeloreto Direcci6n Regional de Agricultura y Direccion Forestal y de Fauna, Iquitos, Peril. NEYMAN, P. E, 1977. Aspects of the ecology and social organization of free ranging cotton-top tamarins Saguinus oedipus and the conservation status of the species. In: The Biology and Conservation of the Callitrichidae, D. G. KLEIMAN(ed.), Smithsonian Univ. Press, Washington, D.C., pp. 39-71. NORCONK, M. A., 1986. Interactions between primate species in a neotropical forest: mixed-species troops of Saguinus mystax and S. fuscicollis (Callitrichidae). Ph.D. thesis, Univ. of California, Los Angeles. OPPENHEIMER, J. R., 1982. Cebus capucinus: home range, population dynamics, and interspecific relationships. In: The Ecology of a Tropical Forest: Seasonal Rhythms and Long-term Changes, E. G. LEIGH,JR, A. S. RAND, & D. M. WINDSOR(eds.), Smithsonian Institution Press, Washington, D.C. pp. 253-272. PERES, C. A., 1986. Costs and benefits of territorial defense in golden lion tamarins, Leontopithecus rosalia. M.S. thesis, Univ. of Florida, Gainesville, Florida. PUSEY, A. E. & C. PACKER, 1987. Dispersal and philopatry. In: Primate Societies, B. B. SMUTS, D. L. CHENEY, R. M. SEYFARTH, R. W. WRANGHAM, & T. Z. STRUHSAKER (eds.), The Univ. of Chicago, Chicago, pp. 250-266. RAMIREZ, M. E, 1989. Feeding ecology and demography of the moustached tamarin Saguinus mystax in northeastern Peru. Ph.D. thesis, City Univ. of New York, New York. ROBINSON, J. G., 1981. Vocal regulation of inter- and intragroup spacing during boundary encounters in the titi monkey, Callicebus moloch. Primates, 22:161 -172. - & C. H. JANSON, 1987. Capuchins, squirrel monkeys, and atelines: socioecological convergence with Old World Primates. In: Primate Societies, B. B. SMUTS, D. L. CHENEY, R. M. SEYFARTH, R. W. WRANGHAM,& Z. Z. STRUHSAKER(eds.), The Univ. of Chicago, Chicago, pp. 69 - 82. - - , P. C. WRIGHT, & W. G. KINZEY, 1987. Monogamous cebids and their relatives: intergroup calls and spacing. In: Primate Societies, B. B. SMUTS, D. L. CHENEY, R. M. SEYFARTH,R. W. WRANGHAM, & Z. T. STRUHSAKER(eds.), The Univ. of Chicago, Chicago, pp. 4 4 - 5 3 . RYLANDS, A. l., 1982. The behaviour and ecology of three species of marmosets and tamarins (Callitrichidae, Primates) in Brazil. Ph.D. thesis. Univ. of Cambridge, Cambridge. - - , 1986. Ranging behaviour and habitat preference of a wild marmoset group, Callithrix humeralifer (Callitrichidae, Primates). J. Zool., 210: 489-514. SAVAGE,A., 1990. The reproductive biology of the cotton-top tamarin (Saguinus oedipus oedipus) in Colombia. Ph.D. thesis, Univ. of Wisconsin, Madison, Wisconsin. SNOWDON, C. Z. & P. SOINI, 1988. The tamarins, genus Saguinus. In: Ecology and Behavior of Neotropical Primates. I1ol. 2. R. A. MITTERMEIER, A. B. RYLANDS, A. COIMBRA-FIEHO,t~r G. A. B. FONSECA(eds.), World Wildlife Fund, Washington, D.C., pp. 2 2 3 - 298. SOINI, P., 1987. Ecology of the saddle-back tamarin Saguinus fuscicollis illigeri on the Rio Pacaya, Northeastern Peru. Folia Primatol., 49:11 - 32. & M. SO~NI, 1982. Distribuci6n geogrfifica y ecologia poblacional de Saguinus mystax (Primates, Callitrichidae). Direcci6n General de Agricultura, Direcci6n Forestal y de Fauna. Informe de Pacaya No. 6. Ordeloreto, Iquitos, Peril. STANFORD, C. B., 1991. Social dynamics of intergroup encounters in the capped langur (Presbytis pileata). Amer. J. Primatol., 25: 3 5 - 4 7 . STEVENSON, M. E 8z A. B. RYLANDS, 1988. The marmosets, genus Callithrix. In: Ecology and Behavior of Neotropical Primates. Vol. 2. R. A. MITTERMEIER, A. B. RYLANDS,A. CO1MBRAFILHO, & G. A. B. FONSECA (eds.), World Wildlife Fund, Washington, D.C., pp. 131-222. -

-


25

SUSSMAN, R. W. & P. A. GARBER, 1987. A new interpretation of the social organization and mating system of the Callitrichidae. Int. J. Primatol., 8: 7 3 - 92.

TERBORGH, J., 1983. Five New World Primates: A Study in Comparative Ecology. Princeton Univ. Press, Princeton, New Jersey.

VAN ROOSMALEN, M. G. M. & L. KLEIN, 1988. The spider monkeys, genus Ateles. In: Ecology and Behavior o f Neotropical Primates. VoL 2. R. A. MITTERMEIER,A. B. RYLANDS, A. COI~BRAFILHO, & G. A. B. FONSECA(eds.), World Wildlife Fund, Washington, D.C., pp. 4 5 5 - 537. WASER, P., 1987. Interactions among primate species. In: Primate Societies, B. B. SMUTS, D. L. CHENEY, R. M. SEVFARTH,R. W. WRANGHAM,& T. T. STRtmSAKER(eds.), The Univ. of Chicago, Chicago, pp. 210-226. & R. H. WILEY, 1979. Mechanisms and evolution of spacing in animals. In: Handbook o f Behavioral Neurobiology. Vol. 3. P. MARLER & J. G. VANDENBERG(eds.), Plenum Press, New York, pp. 169- 223. WATTS, D. E, 1990. Ecology of gorillas and its relation to female transfer in mountain gorillas. Int. J. Primatol., 11" 21-45. WRIGHT, P. C., 1985. The costs and benefits of nocturnality of Aotus trivirgatus (the night monkey). Ph.D. thesis, City Univ. of New York, New York. -

-

--

Received March 23, 1992; Accepted July 9, 1992

Authors' Names and Addresses: P. A. GARBERand J. D. PRUETZ,Department of Anthropology, University of Illinois, 109 Davenport Hall, 607 S. Mathews Avenue, Urbana, Illinois 61801, U. S. A.; J. ISAACSON,Research Associate, Geographical Information Systems Laboratory, Department of Anthropology, University of Illinois, 109 Davenport Hall, 607 S. Mathews Avenue, Urbana, Illinois 61801, U. S. A.